Community Dynamics in a Species-Rich Patch of Old-Growth Forest in a Global Changing Scenario

Acta Botanica Brasilica 27(2): 270-285. 2013.

Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Markus Gastauer1,2 and João Augusto Alves Meira Neto1,2,3

Submitted: 26 April, 2012. Accepted: 16 December, 2012

ABSTRACT Ecological theory predicts that, in mature ecosystems, species richness, the number of individuals and the biomass of individuals will remain in a relatively stable state of equilibrium. The aim of this study was to test that theory. In 2001 and 2010, we conducted censuses of all trees with a circumference at breast height ≥ 10 cm in a one-hectare plot in a seasonal semideciduous old-growth forest in southeastern Brazil. We compared the two censuses in terms of species richness and diversity, computing growth, recruitment and mortality rates, as well as gains and losses of basal area. Between 2001 and 2010, species richness declined from 224 to 218 species and the basal area increased from 37.86 to 40.16 m2 ha−1. Overall turnover (the mean difference between mortality and recruitment) was lower than would be expected for a seasonal semideciduous forest, indicating stability and slight successional advance. This interpretation is supported by the observation that pioneer species and canopy species both showed higher mortality than recruitment. However, uncommon species (< 10 individuals in the 2001 census) showed higher mortality than recruitment and became rarer, whereas most species that were abundant in 2001 became more abundant by 2010. These observations, as well as the decline in species richness, although statistically not significant, match the predictions of ecological theory for scenarios in which formerly contiguous ecosystems become fragmented and the remnants become isolated within the landscape. Nevertheless, further censuses are needed in order to test the idea that the observed patterns are not explained by natural oscillations but are consequences of environmental changes related to human activity.

Key words: Community dynamics, habitat loss, immigration rate, landscape fragmentation, species richness.

Introduction processes of the natural dynamics of the forest (Tabarelli et al. 2004). In addition, changes in resource availability Climate change (IPCC 2007; Matesanz et al. 2010), ha- influence growth, mortality and recruitment of trees within bitat destruction and fragmentation (Wright 2010) threaten forest communities (Ernest et al. 2009). species richness and diversity worldwide. Because tropical Among tropical forests, the Atlantic Forest of Brazil is forests account for the major part of terrestrial biodiversity one of the most diverse ecosystems (Stehmann et al. 2009). (Millennium Ecosystem Assessment 2005), climate change Due to its high degree of endemism and endangered status, is expected to have severe effects on such forests. To outline it is considered a biodiversity hotspot (Myers et al. 2000). and understand the influences of global changes on forest Once covering up to 1,500,000 km2 (Câmara 2005), only communities, their species richness and diversity, it is ne- 11% of the original Atlantic Forest remains, most of it as cessary to conduct long term monitoring studies known small secondary forest patches (Ribeiro et al. 2009). Species- as community dynamics studies (Losos & Leigh Jr. 2004). -rich old-growth forests are extremely rare. Species composition within a given community un- The aim of this study is to test whether the mature tree doubtedly varies over time (Rosenzweig 1995; Hubbell community of the Seu Nico Forest (SNF) shows stability 2001; Magurran 2011). These variations depend on the in the form of dynamic equilibrium over time, in terms disturbance regime (Connell 1978; Molino & Sabatier of community dynamics, such as mortality and recruit- 2001; Machado & Oliveira-Filho 2010), ecological drift and ment rates (Oliveira-Filho et al. 2007); species richness stochasticity (Hubbell 2001). (MacArthur & Wilson 1967); the number of individuals The division of formerly contiguous forests into frag- or zero-sum dynamics (Hubbell 2001); and basal area per ments of variable size and shape also alters the ecological individual (Ernest et al. 2009).

1 Universidade Federal de Viçosa, Departamento de Biologia Vegetal, Laboratório de Ecologia e Evolução das Plantas, Viçosa, MG, Brazil 2 Centro de Ciências Ambientais Floresta-Escola, Frutal, MG, Brazil 3 Author for correspondence: [email protected] Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Methods and is therefore interpreted as spatial turnover, or beta diversity (Condit et al. 1996). For statistical comparison TM Study site of the values, we used Microsoft Excel to perform linear least squares regression. The SNF is a 35 ha patch of species-rich old-growth For both censuses, the biodiversity indices of Simpson forest (20°47’44”S; 42°50’50”W) on the Bom Sucesso Farm, and Shannon-Wiener, as well as Fisher’s alpha, were com- in the town of Viçosa, which is in the state of Minas Gerais, puted with the software EstimateS (Colwell & Coddington Brazil. The owners of the SNF state that it has never been 1994; Colwell 2005). Statistical differences in diversity as logged (Campos et al. 2006). According to the Köppen cli- well as in species richness, basal area and number of indi- mate classification system (Köppen 1948), the climate of the viduals were checked for significance by a two-sample t-test region is type Cwb (Peel et al. 2007), a humid mesothermal after testing for normal distribution by a Shapiro-Wilk test climate with mild, rainy summers and dry winters. The with STATISTCA software, version 7.0 (StatSoft Inc., Tulsa, predominant soils are deeply weathered oxisols, which are OK, USA). Parameters were calculated for each plot. found within a small-scale mosaic of inceptisols on slopes The community dynamics were calculated as proposed and neosols in sedimentation areas of valley bottoms. The by Losos & Lao (2004). To calculate the average growth rate predominant vegetation is characterized as submontane between censuses, the increase in diameter for each tree was seasonal semideciduous forest (Veloso et al. 1991). divided by the interval (in years) between the two censuses. The average growth rate is the average of the growth rates Data collection of all trees meeting the inclusion criteria. The difference in the mortality rate of trees between Within the SNF, a 100 × 100 m (1-ha) area was marked off the censuses is the natural logarithm of the proportional and divided into 100 plots of 10 × 10 m. In an initial census, relationship between the number of trees tagged in the first conducted for all of the plots between October 2000 and March census and that of those surviving to the second census, 2001 (Irsigler 2001), all trees with a circumference at breast divided by the time between the two: height ≥ 10 cm—corresponding to a diameter (DBH) ≥ 3.2 cm—were tagged and identified. Because it is conventional to N In( 1 ) use diameter rather than circumference in the international N literature, we will hereafter refer to the DBH. During a second MR = S T (2) census, carried out between December 2009 and February

2010, we measured the circumference of all surviving indivi- where MR is the mortality rate, NS is the number of survivors duals within the 100 plots. Recruits (individuals that had not (trees that were alive in both censuses), N1 is the NS minus been tagged but met the inclusion criteria) were also tagged and the number of undetected individuals or individuals that identified. Specimens were collected, identified and deposited died between the two censuses, and T is the average interval in the Herbarium of the Federal University of Viçosa (code, between censuses (in years). The rate of tree recruitment VIC). Species nomenclature follows the database compiled by was calculated as follows: Forzza et al. (2012). Species classification follows the Angios- perm Phylogeny Group III guidelines (APG III 2009). N + N In( S R ) N RR = S Data analysis T (3) To compare species richness between the two censuses, where RR is the recruitment rate, and NR is the number of we calculated the species-area relationship using the power new trees appearing between censuses (i.e., recruits). model proposed by Arrhenius (1921) to fit the species- For any given plot, a loss in basal area (defined as the -accumulation curve: area below the 3.2 cm DBH level) resulted from mortality and from stem breakages. To calculate the loss in basal S = cAz (1) area between the two censuses (the total basal area of trees tagged in the first census that had died or whose basal area where S is the number of species; A is the area; and c and z are had otherwise been lost by the time of the second census), constants corresponding to the intercept with the y-axis (c) we employed the following equation: and the slope (z) of the linearized species-area relationship after log transformation of S and A. For the fitting, we AB assessed the average number of species within groups of 2, BA = M (4) loss T 5, 10, 25 and 50 plots, as well as within the study site as a whole (all 100 plots). Only neighboring plots were grouped. where BAloss is the total basal area lost, and ABM is the di- Linearized in logarithmic space, the slope of the species- fference in basal area between the two censuses. Similarly, -area relationship describes the difference between plots a gain in basal area was calculated as follows:

Acta bot. bras. 27(2): 270-285. 2013. 271 Markus Gastauer and João Augusto Alves Meira Neto

BA – BA Lemos (2008), Lima et al. (2010), Lopes et al. (2002), Maran- BA = S2 S1 gain T (5) gon et al. (2007), Metzger et al. (1997), Norden et al. (2009), Nunes et al. (2003), Oliveira-Filho et al. (2004, 2007), Paula et al. (2004), Peixoto et al. (2004), Pinto et al. (2005), Rolim where BAgain is the total basal area gained, BAS2 is the total basal area of the trees surviving from the first to the second census, et al. (1999), Silva et al. (2004), Stranghetti et al. (2003), and Yamamoto et al. (2007). In cases of contradictory informa- and BAS1 is the total basal area of those same individuals in the first census. For the calculation of demographic dynamics, all tion, species were allocated to the strategy indicated in the stems of multi-stemmed individuals were included. greatest number of references. Community dynamics were We calculated demographic dynamics not only for the calculated separately for common species (≤ 9 individuals) community as a whole but also for different size classes, as and uncommon species (≥ 10 individuals). proposed by Losos & Lao (2004): class I (DBH = 3.2-9.9 cm); class II (DBH = 10-29.9 cm); and class III (DBH ≥ 30 cm). Species were classified according to their regeneration, Results stratification and dispersal strategies. Community dynamics were calculated separately for all pioneer and all non- Plot census history -pioneer species following the classification of Swaine & Overall, the number of individuals increased in our plot Whitmore (1988): for understory species, which typically do within the SNF. However, of the 224 species surveyed in 2001, not reach heights above 15 m; for all canopy species, which only 214 remained in 2010. Both changes were less than signi- typically reach heights above 15 m (Liebsch et al. 2008); and ficant (p=0.89 and p=0.81 for the number of individuals and for animal-dispersed and non-animal-dispersed species number of species, respectively). Within the community exa- (Ingle 2003). Information about successional, dispersal and mined, only four new species were recruited between the two dispersal strategies was drawn from the following studies censuses (Table 1). Although this net loss of six species reduced (in alphabetical order, not sorted by relevance): Appolinário the z slope of the species-area relationship (Fig. 1), the differen- et al. (2005), Aquino & Barbosa (2009), Araújo et al. (2005, ces were not significant (z=0.545 ± 0.032 in 2001 and z=0.531 ± 2006), Araujo et al. (2010), Brandão et al. (2009), Cappelatti 0.030 in 2010). The various diversity indices indicated an insig- & Schmitt (2009), Carvalho et al. (2006, 2007), Carvalho nificant loss of tree diversity within the plot (Table 2). The basal & Nascimento (2009), Chagas et al. (2001), Colonetti et al. area increased (from 37.86 m2 ha−1 in 2001 to 40.16 m2 ha−1 (2009), Higuchi et al. (2008a), Leite & Rodrigues (2008), in 2010), albeit insignificantly (p=0.44).

Table 1. Tree species with a diameter at breast height of > 3.2 cm and their ecological guilds identified in two censuses of the tree community in a one-hectare plot within a patch of species-rich old-growth forest (Seu Nico Forest, Viçosa, Brazil).

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) ACHARIACEAE Carpotroche brasiliensis (Raddi) Endl. x x npio/zoo/us ANACARDIACEAE Astronium fraxinifolium Schott x x npio/nzoo/us Astronium graveolens Jacq. x x npio/nzoo/cp Tapirira guianensis Aubl. x x npio/zoo/us Tapirira obtusa (Benth.) J.D. Mitch. x x npio/zoo/cp ANNONACEAE Annona cacans Warm. x x npio/zoo/cp Annona neolaurifolia H. Rainer x x npio/zoo/cp Guatteria australis A. St.-Hil. x x npio/zoo/us Guatteria villosissima Saint-Hilaire x x npio/zoo/us Guatteria sp.1 x x -/zoo/- Guatteria sp. 2 x x -/zoo/- Xylopia brasiliensis Spreng. x x npio/zoo/cp Xylopia sericea A. St.-Hil. x x pio/zoo/us

Continues

272 Acta bot. bras. 27(2): 270-285. 2013. Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) APOCYNACEAE Aspidosperma olivaceum Müll. Arg. x x npio/nzoo/us Aspidosperma polyneuron Müll. Arg. x x npio/nzoo/us Aspidosperma subincanum Mart. x x npio/nzoo/us Himatanthus phagedaenicus (Mart.) Woodson x npio/nzoo/- Tabernaemontana hystrix Steud. x x pio/zoo/us AQUIFOLIACEAE Ilex cerasifolia Reissek x x npio/zoo/us ARALIACEAE Dendropanax cuneatus (DC.) Decne. & Planch. x x npio/zoo/sb Schefflera morototoni (Aubl.) Maguire et al. x x pio/zoo/cp ARECACEAE Astrocaryum aculeatissimum (Schott) Burret x x npio/zoo/us Euterpe edulis Mart. x x npio/zoo/us Syagrus romanzoffiana (Cham.) Glassman x npio/zoo/cp ASTERACEAE Vernonanthura diffusa (Less.) H.Rob. x x pio/nzoo/cp BIGNONIACEAE Handroanthus chrysotrichus (Mart. ex A. DC.) Mattos x x npio/nzoo/us Jacaranda macrantha Cham. x x npio/nzoo/cp Sparattosperma leucanthum (Vell.) K. Schum. x x npio/nzoo/us BURSERACEAE Protium heptaphyllum (Aubl.) Marchand x x npio/zoo/cp Protium warmingianum Marchand x x npio/zoo/cp Trattinnickia ferruginea Kuhlm. x x -/zoo/cp CANNABACEAE Celtis iguanaea (Jacq.) Sarg. x pio/zoo/us CARDIOPTERIDACEAE Citronella paniculata (Mart.) R.A. Howard x x npio/zoo/us CARICACEAE Jacaratia cf. heptaphylla (Vell.) A. DC. x x npio/zoo/us Jacaratia spinosa (Aubl.) A. DC. x npio/zoo/cp CELASTRACEAE Maytenus floribunda Reissek x x npio/zoo/us Maytenus robusta Reissek x x npio/zoo/us Maytenus salicifolia Reissek x x npio/zoo/us Salacia elliptica (Mart. ex Schult.) G. Don x x npio/zoo/us CHRYSOBALANACEAE Hirtella hebeclada Moric. ex DC. x x npio/zoo/cp Licania belemii Prance x x -/zoo/cp CLUSIACEAE Kielmeyera albopunctata Saddi x x -/-/cp Garcinia brasiliensis Mart. x x npio/zoo/us

Continues

Acta bot. bras. 27(2): 270-285. 2013. 273 Markus Gastauer and João Augusto Alves Meira Neto

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) Tovomita glazioviana Engl. x x npio/zoo/cp Tovomitopsis saldanhae Engl. x x npio/zoo/cp COMBRETACEAE Terminalia glabrascens Mart. x x npio/nzoo/us CORDIACEAE Cordia sellowiana Cham. x x npio/zoo/cp ELAEOCARPACEAE Sloanea hirsuta (Schott) Planch ex Benth. x x npio/zoo/us ERYTHROXYLACEAE Erythroxylum daphnites Mart. x x -/zoo/us Erythroxylum pelleterianum A. St.-Hil. x x npio/zoo/us EUPHORBIACEAE Alchornea glandulosa Poepp. & Endl. x x pio/zoo/cp Alchornea triplinervia (Spreng.) Müll. Arg. x x npio/zoo/cp Aparisthmium cordatum (A.Juss.) Baill. x x npio/nzoo/us Croton floribundus Spreng. x x pio/nzoo/cp Croton hemiargyreus Müll. Arg. x ///// Mabea fistulifera Mart. x x pio/nzoo/cp Maprounea guianensis Aubl. x x npio/nzoo/cp Sapium glandulosum (L.) Morong x x pio/zoo/cp Euphorbiaceae sp.1 x x -/-/- Euphorbiaceae sp.2 x x -/-/- Euphorbiaceae sp.3 x x -/-/- FABACEAE Andira fraxinifolia Benth. x x npio/zoo/us Apuleia leiocarpa (Vogel) J.F. Macbr. x x npio/nzoo/cp Caesalpinaceae sp. x x -/-/- Copaifera langsdorffii Desf. x x npio/zoo/cp Dalbergia nigra (Vell.) Allemao ex Benth. x x npio/nzoo/cp Hymenaea sp. x x -/-/- Inga capitata Desv. x x npio/zoo/cp Inga cylindrica (Vell.) Mart. x x npio/zoo/cp Inga vera Willd. x x npio/zoo/cp Inga sp.1 x x -/zoo/cp Inga sp. 2 x -/-/- Lonchocarpus cultratus (Vell.) A.M.G. Azevedo & H.C. Lima x x npio/nzoo/cp Machaerium caratinganum Kuhlm. & Hoehne x x npio/nzoo// Machaerium nyctitans (Vell.) Benth. x x npio/nzoo/cp Machaerium sp. x x -/nzoo/- Melanoxylon brauna Schott x x npio/nzoo/cp Moldenhawera sp. x -/-/- Ormosia arborea (Vell.) Harms x x npio/zoo/cp Peltophorum dubium (Spreng.) Taub. x x npio/zoo/cp

Continues

274 Acta bot. bras. 27(2): 270-285. 2013. Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) Piptadenia gonoacantha (Mart.) J.F. Macbr. x x pio/nzoo/cp Pseudopiptadenia contorta (DC.) G.P. Lewis & M.P. Lima x x npio/nzoo/cp Swartzia acutifolia Vogel x x npio/zoo/cp Swartzia myrtifolia Sm. x x npio/zoo/us HUMIRIACEAE Vantanea obovata (Nees & Mart.) Benth. x -/zoo/us LACISTEMACEAE Lacistema pubescens Mart. x x npio/zoo/us LAURACEAE Aniba firmula (Nees & C. Mart.) Mez x x npio/zoo/cp Cinnamomum glaziovii (Mez) Kosterm. x x npio/zoo/cp Cryptocarya moschata Nees & C. Mart. ex Nees x x npio/zoo/cp Nectandra lanceolata Nees & Mart. x x npio/zoo/cp Nectandra oppositifolia Nees x x npio/zoo/cp Ocotea corymbosa (Meisn.) Mez x x npio/zoo/cp Ocotea dispersa (Nees) Mez x x npio/zoo/us Ocotea odorifera (Vell.) Rohwer x x npio/zoo/cp Ocotea pulchella (Nees & Mart.) Mez x x npio/zoo/us Ocotea silvestris Vattimo-Gil x x npio/zoo/us Ocotea sp. x x -/zoo/- Persea wildenowii Kosterm. x npio/zoo/cp Phyllostemonodaphne geminiflora (Mez) Kosterm. x x npio/zoo/us Urbanodendron verrucosum (Nees) Mez x x npio/zoo/us Lauraceae sp.1 x x -/-/- Lauraceae sp.2 x x -/-/- Lauraceae sp.3 x -/-/- LECYTHIDACEAE Cariniana estrellensis (Raddi) Kuntze x x npio/nzoo/cp Cariniana legalis (Mart.) Kuntze x x npio/nzoo/cp LYTHRACEAE Lafoensia glyptocarpa Koehne x x npio/-/cp MALVACEAE Ceiba speciosa (A. St.-Hil.) Ravenna x x npio/nzoo/cp Eriotheca candolleana (K. Schum.) A. Robyns x x npio/nzoo/us Luehea grandiflora Mart. & Zucc. x x npio/nzoo/us Sterculia curiosa (Vell.) Taroda x x npio/zoo/cp MELASTOMATACEAE Miconia brunnea DC. x x -/zoo/us Miconia budlejoides Triana x x npio/zoo/us Miconia cinnamomifolia (DC.) Naudin x x pio/zoo/us Miconia minutiflora (Bonpl.) DC. x x -/zoo/cp Miconia tristis Spring x x npio/zoo/us Mouriri glazioviana Cogn. x x npio/zoo/us

Continues

Acta bot. bras. 27(2): 270-285. 2013. 275 Markus Gastauer and João Augusto Alves Meira Neto

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) MELIACEAE Cabralea canjerana (Vell.) Mart. x x npio/zoo/cp Cedrela fissilis Vell. x x npio/zoo/cp Guarea fistulosa W. Palacios x x -/zoo/cp Guarea guidonia (L.) Sleumer x x npio/zoo/cp Guarea macrophylla Vahl x x npio/zoo/cp Guarea pendula R.da Silva Ramalho, A.L. Pinheiro & T.D. Penn. x x npio/zoo/us Trichilia catigua A. Juss. x x npio/zoo/us Trichilia emarginata (Turcz.) C. DC. x x npio/zoo/us Trichilia lepidota Mart. x x npio/zoo/cp Trichilia pallida Sw. x x npio/zoo/cp MONIMIACEAE Mollinedia schottiana (Spreng.) Perkins x x npio/zoo/us Monimiaceae sp. x -/-/- MORACEAE Clarisia ilicifolia (Spreng.) Lanj. & Rossberg x x npio/zoo/us Brosimum guianense (Aubl.) Huber x x npio/zoo/cp Ficus gomelleira Kunth & C.D. Bouché x x npio/zoo/cp Ficus luschnathiana (Miq.) Miq. x x npio/zoo/cp Ficus enormis Mart. ex Miq. x x npio/zoo/cp Helicostylis tomentosa (Poepp. & Endl.) Rusby x x npio/zoo/cp Maclura tinctoria (L.) D. Don ex Steud. x x npio/zoo/cp Naucleopsis oblongifolia (Kuhlm.) Carauta x x npio/zoo/cp Sorocea bonplandii (Baill.) W.C. Burger, Lanj. & Wess. Boer x x npio/zoo/us Sorocea hilariana Gaudich. x x Npio/zoo/us MYRISTICACEAE Virola bicuhyba (Schott ex. Spreng.) Warb. x x npio/zoo/cp Virola gardneri (A. DC.) Warb. x x npio/zoo/cp MYRTACEAE Calyptranthes brasiliensis Spreng. x x npio/zoo/us Campomanesia xanthocarpa (Mart.) O. Berg x x npio/zoo/us Eugenia cf. lambertiana DC. x x npio/zoo/us Eugenia dodonaeifolia Cambess. x x npio/zoo/us Eugenia florida DC. x x npio/zoo/us Eugenia leptoclada O.Berg x x npio/zoo/us Marlierea excoriata Mart. x x npio/zoo/us Marlierea suaveolens Cambess. x x npio/zoo/us Marlierea cf. teuscheriana (O.Berg) D.Legrand x x npio/zoo/us Myrcia anceps (Spreng.) O. Berg x x npio/zoo/us Myrciaria floribunda (H.West ex Willd.) O.Berg x x npio/zoo/us Myrcia pallida (Cambess.) O. Berg x x npio/zoo/- Myrcia pubipetala Miq. x x npio/zoo/us Myrcia splendens (Sw.) DC. x x npio/zoo/us Myrcia sp. x x -/zoo/- Neomitranthes sp. x x -/zoo/us Plinia cf. grandifolia (Mattos) Sobral x x npio/zoo/us Psidium cf. oblongatum O. Berg x x -/zoo/- Myrtaceae sp. x x -/zoo/-

Continues

276 Acta bot. bras. 27(2): 270-285. 2013. Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) NYCTAGINACEAE Guapira hirsuta (Choisy) Lundell x x npio/zoo/us Guapira opposita (Vell.) Reitz x x npio/zoo/us Pisonia ambigua Griseb. x x npio/zoo/cp Nyctaginaceae sp. x x -/zoo/- OCHNACEAE Ouratea polygyna Engl. x x npio/zoo/us OLACACEAE Heisteria silvianii Schwacke x x npio/zoo/us Tetrastylidium grandiflorum (Baill.) Sleumer x x npio/zoo/us Oleaceae sp. x x -/zoo/- PERACEAE Pera glabrata (Schott) Poepp. ex Baill. x x npio/zoo/cp PHYLLANTHACEAE Hieronyma alchorneoides Allemão x x npio/zoo/cp Margaritaria nobilis L. f. x x npio/zoo/cp PIPERACEAE Piper arboreum Aubl. x x npio/zoo/us Piper gigantifolium C. DC. x x -/zoo/us PRIMULACEAE Cybianthus fuscus Mart. x -/zoo/- Myrsine umbellata Mart. x x npio/zoo/us Stylogyne pauciflora (Mart. & Miq.) Mez x x -/zoo/us RHAMNACEAE Colubrina glandulosa Perkins x x npio/zoo/cp ROSACEAE Prunus myrtifolia (L.) Urb. x x npio/zoo/cp RUBIACEAE Alseis floribunda Schott x x npio/zoo/us Amaioua guianensis Aubl. x x npio/zoo/us Bathysa cuspidata (St. Hil.) Hook.f. ex K.Schum. x x npio/aut/us Bathysa nicholsonii K. Schum. x x npio/aut/us Genipa americana L. x x npio/zoo/cp Guettarda viburnoides Cham. & Schltdl. x x npio/zoo/us Ixora gardneriana Benth. x x npio/zoo/us Psychotria carthagenensis Jacq. x x npio/zoo/us Psychotria rhytidocarpa Müll. Arg. x x npio/zoo/us Psychoria myriantha Müll. Arg. x x npio/zoo/us Psychotria nuda (Cham. & Schltdl.) Wawra x x npio/zoo/us Psychotria vellosiana Benth. x x npio/zoo/us Psychotria sp. x x -/zoo/- Randia ferox (Cham. & Schltdl.) DC. x x npio/zoo/us Rudgea jasminoides (Cham.) Müll.Arg. x x npio/zoo/us Rubiaceae sp. x -/zoo/- RUTACEAE Hortia brasiliana Vand. ex DC. x x -/zoo/cp Zanthoxylum rhoifolium Lam. x x npio/zoo/us

Continues

Acta bot. bras. 27(2): 270-285. 2013. 277 Markus Gastauer and João Augusto Alves Meira Neto

Table 1. Continuation.

FAMILY 2001 2010 Ecological guild Species (n = 224) (n = 218) SABIACEAE Meliosma itatiaiae Urb. x x -/zoo/us SALICACEAE Casearia arborea (Rich.) Urb. x x npio/zoo/cp Casearia decandra Jacq. x x npio/zoo/cp Casearia gossypiosperma Briq. x x npio/nzoo/us Casearia sylvestris Sw. x x pio/zoo/us Casearia ulmifolia Vahl ex Vent. x x npio/zoo/us Macrothumia kuhlmannii (Sleumer) M.H.Alford x x -/zoo/cp Prockia crucis P. Browne ex L. x x npio/zoo/us Xylosma prockia (Turcz.) Turcz. x x npio/zoo/us Salicaceae sp. x x -/zoo/- SAPINDACEAE Allophylus edulis (A. St.-Hil. et al.) Hieron. ex Niederl. x x npio/zoo/us Cupania vernalis Cambess. x x npio/zoo/cp Matayba elaeagnoides Radlk. x x npio/zoo/cp SAPOTACEAE Chrysophyllum gonocarpum (Mart. & Eichler ex Miq.) Engl. x x npio/zoo/cp Chrysophyllum lucentifolium Cronquist x x npio/zoo/us Chrysophyllum cf. marginatum (Hook. & Arn.) Radlk. x x npio/zoo/cp Chrysophyllum sp. x x -/zoo/- Pouteria caimito (Ruiz & Pav.) Radlk. x x npio/zoo/cp Pradosia lactescens (Vell.) Radlk. x x npio/zoo/cp SIPARUNACEAE Siparuna guianensis Aubl. x x npio/zoo/us Siparuna reginae (Tul.) A. DC. x x npio/zoo/us SOLANACEAE Brunfelsia uniflora (Pohl) D. Don x x npio/zoo/us Cestrum mariqitense Kunth x x -/zoo/us Cestrum sp. x x -/zoo/- Solanaceae sp. x x -/zoo/- URTICACEAE Cecropia hololeuca Miq. x x pio/zoo/cp Coussapoa floccosa Akkermans & C.C. Berg x x -/zoo/us Coussapoa microcarpa (Schott) Rizzini x x npio/zoo/cp Pourouma guianensis Aubl. x x pio/zoo/cp VOCHYSIACEAE Qualea multiflora Mart. x x npio/zoo/cp UNKNOWN FAMILY Unidentified sp.1 x x -/-/- Unidentified sp.2 x x -/-/- Unidentified sp.3 x -/-/- 218 species

pio – pioneer; npio – non-pioneer; zoo – zoochorous (animal-dispersed); nzoo – non-zoochorous (non-animal-dispersed); us – understory; cp – canopy.

278 Acta bot. bras. 27(2): 270-285. 2013. Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Species ranks from both censuses showed an s-shaped curve (Fig. 2). Due to lower species richness and higher abundance of common species in 2010, the curve trended downward, although the slope decreased only slightly from 2001 to 2010 (from −0.0089 ± 0.0009 to −0.0083 ± 0.0008). Mortality rates were high for some of the uncommon species, such as Vernonanthura diffusa (15.4% yr−1) and Astronium fraxinifolium (13.1% yr−1), whose populations declined. The populations of other species increased consi- derably, with above-average recruitment rates. Examples are Siparuna reginae (23.1% yr−1) or Eugenia florida (13.4% yr−1). Among the most abundant species, recruitment rates were above average for Siparuna guianensis (3.1% yr−1), Euterpe edulis (4.1% yr−1), Virola gardneri (3.3% yr−1) and Eugenia cf. lambertiana (3.9% yr−1), whereas mortality rates were above average for Bathysa nicholsonii (2.6% yr−1), S. guia- Figure 1. Rarefaction of the species accumulation curves for censuses conducted nensis (2.4% yr−1), Pourouma guianensis and (2.5% yr−1) and in 2001 and 2010 in a one-hectare plot within a patch of species-rich old-growth Casearia ulmifolia (2.4% yr−1). forest (Seu Nico Forest, Viçosa, Brazil). Species-area relationship, fitted by the power model, does not differ significantly between 2001 and 2010, in terms of the log number of species (0.545 ± 0.032 vs. 0.531 ± 0.030) or the log area (+0.233 ± 0.099 vs. +0.273 ± 0.093). Discussion Within the 1 ha plot of the SNF evaluated, we obtained Table 2. Changes in tree species diversity between two censuses, conducted nine years apart, in a one-hectare plot within a patch of species-rich old-growth low values for the key features of community dynamics, forest (Seu Nico Forest, Viçosa, Brazil). such as recruitment, mortality and growth rates, as well as losses and gains of basal area (Leigh et al. 2004; Thompson Diversity index 2001 2010 p* et al. 2004). Within the Atlantic Forest and the Cerrado Fisher’s alpha 59.69 ±2.25 57.2 ± 2.17 0.27 domains, mortality and recruitment rates are generally Shannon-Wiener 4.42 4.37 0.86 higher for flooded gallery forests (Lopes & Schiavini 2007; Simpson 43.08 39.87 0.71 Higuchi et al. 2008b; Fontes & Walter 2011) than for non-

*Two-sample t-test. -flooded gallery forests (Pinto 2002; Oliveira-Filho & Felfili 2008), for seasonal deciduous forests (Carvalho & Felfili, 2011), for seasonal semideciduous forests (Apollinario et al. 2005; Oliveira-Filho et al. 1997, 2007; Silva & Araújo 2009; Community dynamics Machado & Oliveira-Filho 2010) and for evergreen forests Between the first and second censuses, the number (Rolim et al. 1999; Saiter et al. 2011). of individuals increased because recruitment exceeded The mortality and recruitment rates reported in the mortality (Table 3). In terms of basal area, gains surpassed literature are higher than those observed for our study site, losses, resulting in a net gain from 2001 to 2010. Among indicating that there was high stability in the SNF. This the common species, mortality and recruitment rates were stability is congruent with the findings reported by Saiter nearly identical. However, among the uncommon species, et al. (2011) for other old-growth, mature forests. the mortality rate was higher than was the recruitment For the SNF plot evaluated, size class was not found rate. In comparison with that observed for the community to correlate with mortality or recruitment. In disturbed as a whole, mortality was disproportionately high among forests, mortality is typically higher among the smaller size the pioneer and non-animal dispersed species. Among the classes usually because of the effect known as self-thinning understory species, recruitment exceeded mortality. (Oliveira-Filho et al. 2007; Saiter et al. 2011). However, the observations that mortality exceeded recruitment among pioneer species and recruitment exceeded mortality among Population dynamics animal-dispersed species, as well as among understory Of the nine species that were the most abundant in species, indicates a slight successional advance of the SNF 2001, eight increased in abundance, only Bathysa nicholsonii as a mature forest, making it even more representative of being less represented in 2010 than in 2001 (Table 4). Of the an old-growth forest (Liebsch et al. 2008). 20 species with the highest basal areas, 10 increased their Turnover rates were high only for some of the uncom- basal area by more than 10%. In five species, there was a mon species (data not shown). Due to a low number of moderate to high increase in basal area, which decreased individuals, even small alterations within these populations in another five species. result in high rates. Among the twenty most abundant

Acta bot. bras. 27(2): 270-285. 2013. 279 Markus Gastauer and João Augusto Alves Meira Neto

Table 3. Tree demographic dynamics in two censuses, conducted nine years apart (in 2001 and 2010), in a one-hectare plot within a patch of species-rich old-growth forest (Seu Nico Forest, Viçosa, Brazil).

Basal area Growth Mortality Recruitment Category Lost Gained (mm yr−1) (% yr−1) (% yr−1)(m2 ha−1 yr−1)(m2 ha−1 yr−1) All 1.12 1.65 1.84 0.47 0.73 Size class (cm DBH) 3.2-9.9 0.81 1.88 2.69 0.79 0.15 10-29.9 1.79 0.98 2.07 0.15 0.32 ≥30 2.10 1.75 2.48 0.24 0.26 Abundance class* Uncommon (≤ 9 species) 1.31 2.09 1.78 0.18 0.22 Common (≥ 10 species) 1.08 1.54 1.56 0.29 0.51 Successional group Pioneer 1.56 3.37 1.74 0.09 0.04 Non-pioneer 1.11 1.59 1.84 0.39 0.69 Disperal group Animal-dispersed 0.62 1.48 1.73 0.34 0.59 Non-animal-dispersed 1.24 2.86 0.61 0.13 0.12 Vertical position Understory 0.49 1.73 3.53 0.14 0.33 Canopy 0.91 1.44 0.99 0.32 0.39

DBH – diameter at breast height. *Refers to the 2001 census.

species, turnover rates were above average for only a few, work (2001). In addition, because the amount of biomass including S. guianensis, E. edulis, V. gardneri, and E. cf. supported within an ecosystem depends on energy and lambertiana, which are non-pioneer, animal-dispersed resource inputs (Ernest et al. 2009), the increase in basal species, the occurrence of which indicates forest matura- area might be explained by increased resource availability tion (Liebsch et al. 2008). Several of the most abundant (Lewis et al. 2004), perhaps due to climate change (IPCC species showed high mortality rates, the highest being for 2007). This is alarming, because the same tendencies have P. guianensis. Because P. guianensis is a pioneer species, a recently been observed in other regions of the Atlantic decline in its population is also indicative of the ongoing Forest (Higuchi et al. 2008b; Carvalho & Felfili 2011; successional change in the SNF. Saiter et al. 2011). Although the recruitment and mortality rates, as well Regarding the decline in species richness, Felfili et al. as the gains and losses of basal area, indicate stability and (2000) stressed the difficulty in interpreting what they slight successional advance for the tree community of the referred to as “pseudoextinction”, because species might SNF, our comparison of the two censuses revealed some still be present within the community in form of seeds, tendencies that merit discussion. As species richness seedlings or treelets that have not yet met the inclusion and diversity declined, common species became more criterion. However, if a net loss of six species represents a common, while rare species became rarer. In addition, natural oscillation of the tree community, a net gain of six the number of individuals and the total basal area both species in nine years, perhaps in the next census or in similar increased. The fact that those tendencies were not signi- studies, could be expected. We are not aware of any studies ficant might be due to the small sample size. However, it is reporting such net gains in primary or late secondary forests; also possible that they were stochastic, describing only the on the contrary, most dynamic studies conducted to date natural oscillations within the dynamic equilibrium of the have also reported declining numbers of species (Oliveira- seasonal semideciduous Atlantic Forest (Rees et al. 2001; -Filho et al. 1997; Bunyavejchewin et al. 2004; Lee et al. Lopes & Schiavini 2007; Paiva et al. 2007). Nevertheless, 2004; Leigh et al. 2004; Thompson et al. 2004; Werneck & an increase in the number of individuals contradicts the Franceschinelli 2004; Higuchi et al. 2008a, 2008b; Machado zero-sum assumptions made by Hubbell in a theoretical & Oliveira-Filho 2010).

280 Acta bot. bras. 27(2): 270-285. 2013. Community dynamics in a species-rich patch of old-growth forest in a global changing scenario

Table 4. Species ranking, by species abundance (left half) and by basal area (right half), from the second of two censuses conducted in a one-hectare plot within a patch of species-rich old-growth forest (Seu Nico Forest, Viçosa, Brazil).

Number of trees Basal area

Rank 2001 2010 2001 2010 (2010) % of % of Species Diff. trees Species Diff. trees nn(2010) (m2 ha−1)(m2 ha−1) (2010)

Ficus gomelleira Kunth 1 Siparuna guianensis Aubl. (Siparunaceae) 240 254 + 10.04 3.097 3.405 ++ 0.04 & C.D. Bouché (Moraceae)

Protium warmingiana Pseudopiptadenia contorta (DC.) 2 115 121 + 4.784 2.988 3.082 + 1.78 March, L. (Burseraceae) G.P. Lewis & M.P. Lima (Fabaceae)

Sorocea bonplandii (Baill.) W.C. Burger, Virola gardneri (A. DC.) 3 101 107 + 4.231 1.876 2.221 +++ 3.08 Lanj. &Wess. Boer (Moraceae) Warb. (Myristicaceae)

Myrciaria floribunda (H.WestexWilld.) 4 77 101 +++ 3.994 Guatteria nigrescens Mart. (Annonaceae) 1.709 1.912 +++ 2.65 O.Berg (Myrtaceae)

Sterculia chicha A. St.-Hil. 5 Euterpe edulis Mart. (Arecaceae) 68 90 +++ 3.559 1.948 1.840 −− 0.47 Ex Turpin (Malvaceae)

Virola gardneri (A. DC.) Ceiba speciosa (A. St.-Hil.) 6 59 78 +++ 3.084 1.301 1.371 ++ 0.04 Warb. (Myristicaceae) Ravenna (Malvaceae)

Helicostylis tomentosa Protium warmingiana 7 72 73 + 2.887 1.093 1.292 +++ 4.78 (Poepp. &Endl.) Rusby (Moraceae) March, L. (Burseraceae)

Sorocea bonplandii (Baill.) W.C. Burger, 8 Guatteria nigrescens Mart. (Annonaceae) 65 67 + 2.649 1.125 1.258 +++ 4.23 Lanj. &Wess. Boer (Moraceae)

9 Bathysa nicholsonii K. Schum. (Rubiaceae) 71 60 −−− 2.372 Astronium graveolens Jacq. (Anacardiaceae) 1.004 0.974 − 0.51

10 Marlieria excoriata Mart. (Myrtaceae) 61 59 − 2.333 Ocotea silvestris Vattimo (Lauraceae) 0.647 0.822 +++ 0.95

Phyllostemonodaphne geminiflora 11 62 59 − 2.333 Casearia ulmifolia Vahl ex Vent. (Salicaceae) 0.682 0.728 ++ 1.19 (Mez) Kosterm. (Lauraceae)

Brosimum guianense (Aubl.) 12 48 49 + 1.938 Pourouma guianensis Aubl. (Urticaceae) 0.815 0.659 −−− 1.23 Huber(Moraceae)

Helicostylis tomentosa (Poepp. &Endl.) 13 Eugenia cf. lambertiana O. Berg (Myrtaceae) 37 47 +++ 1.858 0.552 0.643 +++ 2.89 Rusby (Moraceae)

Pseudopiptadenia contorta (DC.) 14 56 45 −− 1.779 Euterpe edulis Mart. (Arecaceae) 0.507 0.638 +++ 3.56 G.P. Lewis & M.P. Lima (Fabaceae)

Trichilia emarginata 15 33 35 + 1.384 Bathysa nicholsonii K. Schum. (Rubiaceae) 0.679 0.595 −−− 2.37 (Turcz.) C. DC. (Meliaceae)

Brosimum guianense 16 Trichilia catigua A. Juss. (Meliaceae) 36 34 −− 1.344 0.524 0.594 +++ 1.94 (Aubl.) Huber (Moraceae)

Alseis floribunda (Standl.) 17 26 31 +++ 1.226 Siparuna guianensis Aubl. (Siparunaceae) 0.573 0.577 + 10.04 Steyerm. (Rubiaceae)

18 Pourouma guianensis Aubl. (Urticaceae) 35 31 −−− 1.226 Guarea macrophylla Vahl (Meliaceae) 0.592 0.555 −− 0.59

Virola oleifera (Schott) 19 Casearia ulmifolia Vahl ex Vent. (Salicaceae) 36 30 −−− 1.186 0.472 0.554 +++ 0.71 A.C. Sm. (Myristicaceae)

Chrysophyllum lucentifolium 20 27 28 + 1.107 Ocotea odorífera Rohwer (Lauraceae) 0.448 0.544 +++ 1.07 Cronquist (Sapindaceae)

Diff. – difference; + – moderate increase (< 5%); ++ – considerable increase (5-10%); +++ significant increase (> 10%), − – moderate loss (< 5%); −− – considerable loss (5-10%); −−− – significant loss (> 10%).

Acta bot. bras. 27(2): 270-285. 2013. 281 Markus Gastauer and João Augusto Alves Meira Neto

our case measured as pseudoextinction (Felfili et al. 2000; Carvalho & Felfili 2011), continues unchanged, which causes ongoing species loss. In this scenario, species loss in the SNF will continue until a new equilibrium is reached between extinction and reduced immigration rate. These theoretical explications of the species loss observed in the SNF are congruent with the findings of Hubbell (2001), who ran simulations of the distribution of species abundance in local communities. In isolated stands (communities with reduced immigration rates), common species become more common and rare species become rarer, as was observed in the SNF plot evaluated here. This is a vicious cycle: due to isolation, common species become more common in the

Figure 2. Species rank from censuses conducted in 2001 and 2010 in a one- local community but also increase their abundance in the -hectare plot within a patch of species-rich old-growth forest (Seu Nico Forest, metacommunity. Because abundance in the local commu- Viçosa, Brazil). nity, even in isolation, still depends on species abundance in the metacommunity, this commonness of already common species further increases metacommunity abundance. Because these observations have been made within a Increased mortality of uncommon species supports the landscape that was logged recently (about 150 years ago) categorization of the species loss observed in the SNF as and is now fragmented, they should be discussed from a time-delayed species loss after landscape fragmentation. metacommunity perspective. According to the species-area As shown above, our tree community dynamics study relationship, one of the most widely studied patterns in of the SNF indicated stability and low dynamics in this ecology (Tjørve 2003; Martin & Goldenfeld 2006; Colwell unique patch of primary forest. The slight, insignificant et al. 2012), habitat area loss causes species loss (Pimm & decline in species richness and the increase in basal area Raven 2000; Ney-Nifle & Mangel 2000; Fischer 2000; He & might be due to natural oscillations around an equilibrium Hubbell 2011). However, decades of research on species-area value but might also be interpreted as consequences of relationships have also revealed that species richness is lower environmental changes that are currently affecting vegeta- on islands than on contiguous land masses of the same area tion and will do so into the future. Future censuses in the (Rosenzweig 1995; Lomolino 2001). Because landscape same SNF plot showing similar tendencies will support our fragmentation might be interpreted as the transformation hypothesis that the changes observed in this, one of the last of former contiguous habitats into small patches, forming old-growth forest remnants in the region, are due to human continental islands, theory predicts that a secondary, delayed activity worldwide. loss of species should occur after landscape fragmentation (Rosenzweig 1995). According to the theory of biogeography, species rich- Acknowledgments ness at a given site is achieved by maintaining equilibrium among the rates of immigration, speciation (Hubbell 2001) We are grateful to David Teixeira Irsigler for carrying and extinction (MacArthur & Wilson 1967). In the present out the first census in the SNF. This study received financial study more species disappeared from the community than support from Suzano Pulp and Paper in the form of a doc- were recruited. Therefore, we might assume that there was toral scholarship grant to M.G. Authors also thank CNPq, a disturbance of this equilibrium, indicating problems FAPEMIG, MCTI and SECTES-MG for financial support. with the immigration of propagules of new species to the J.A.A.M.N. has research scholarship of CNPq. SNF. Against this conclusion stands the observation that recruitment rates were higher for animal-dispersed species than for non-animal-dispersed species (Table 3), and that References the four new species were animal-dispersed. This indicates APG (Angiosperm Phylogeny Group) III. 2009. An update of the Angio- that an adapted fauna is actually dispersing seeds and fruits sperm Phylogeny Group classification for the orders and families of within the fragment and should guarantee genetic exchange flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105-121. between the SNF and neighboring fragments. However, as Appolinário, V.; Oliveira Filho, A.T. & Guilherme F.A.G. 2005. Tree popula- research activities in the last decades have shown, these tion and community dynamics in a Brazilian tropical semideciduous secondary fragments are less species-rich (Lopes et al. 2002; forest. Revista Brasileira de Botânica 28(2): 347-360. Meira-Neto & Martins 2002; Paula et al. 2004; Ribas et al. Aquino, C. & Barbosa, L.M. 2009. Classes sucessionais e síndromes de dis- et al. persão de espécies arbóreas e arbustivas existentes em vegetação ciliar 2004; Ferreira Jr. 2007). This reduces the richness of remanescente (Conchal, SP), como subsídio para avaliar o potencial arriving seeds and therefore the immigration rate of propa- do fragmento como fonte de propágulos para enriquecimento de áreas gules from new species. Nevertheless, natural extinction, in revegetadas no Rio Mogi-Guaçu, SP. Revista Árvore 33(2): 349-358.

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